369 Altitudinal migration in American (Cinclus mexicanus): Do migrants produce higher quality offspring?

R.H. Mackas, D.J. Green, I.B.J. Whitehorne, E.N. Fairhurst, H.A. Middleton, and C.A. Morrissey

Abstract: Breeding at high elevations can favour life-history strategies in which parents shift to investing in higher quality rather than higher numbers of offspring. In American Dippers (Cinclus mexicanus Swainson, 1827), altitudinal migrants produce fewer fledglings than sedentary individuals (residents) that breed at lower elevations. We examined whether mi- grants compensate for their lower fecundity by providing their offspring with a higher quality diet and (or) more food, and producing higher quality offspring. Nestling diet was assessed using observations and stable isotope analysis of feathers grown during the nestling period. Nestling quality was assessed using a condition index (residuals from a mass–tarsus re- gression) and postfledging survival. We found that migrants fed their offspring less fish, and despite having higher feeding rates, had lower energetic provisioning rates than residents. Migrants also produced offspring that were in worse condition and had lower postfledging survival. This study found no evidence that altitudinal migration is associated with a trade-off favouring the production of smaller numbers of higher quality young. Instead our data provide support for the hypothesis that altitudinal migration in American Dippers is an outcome of competition for limited nest sites at lower elevations that forces some individuals to move to higher elevations to breed. Re´sume´ : La reproduction aux hautes altitudes peut favoriser des strate´gies de´mographiques dans lesquelles les parents in- vestissent dans des rejetons de plus grande qualite´ plutoˆt que dans un nombre plus e´leve´ de rejetons. Chez le cincle d’Ame´rique (Cinclus mexicanus Swainson, 1827), les individus qui migrent en altitude produisent moins de petits a` l’envol que les individus se´dentaires (re´sidants) des altitudes plus basses. Nous ve´rifions si les migrateurs compensent leur fe´con- dite´ re´duite en procurant a` leurs rejetons un meilleur re´gime alimentaire ou un re´gime plus abondant et en produisant ainsi des petits de meilleure qualite´.Lere´gime alimentaire des petits au nid a pu eˆtre de´termine´ par observation directe et par analyse des isotopes stables dans les plumes e´labore´es durant la pe´riode au nid. La qualite´ des petits au nid a e´te´ mesure´e par un indice de condition (re´sidus de la re´gression de la masse sur le tarse) et par la survie apre`s l’envol. Les migrateurs apportent moins de poissons a` leurs rejetons et, malgre´ des taux d’alimentation plus e´leve´s, ils ont des taux d’approvision- nement en e´nergie infe´rieurs a` ceux des re´sidants. Les migrateurs produisent aussi des petits en moins bonne condition dont la survie apre`s l’envol est infe´rieure. Notre e´tude n’offre aucune indication que la migration en altitude comporte un compromis favorisant la production de petits moins nombreux mais de meilleure qualite´. Au contraire, nos donne´es ap- puient l’hypothe`se selon laquelle la migration en altitude chez les cincles d’Ame´rique re´sulte de la compe´tition pour un nombre limite´ de sites de nidification aux altitudes infe´rieures, ce qui oblige certains individus a` se de´placer vers les altitu- des supe´rieures pour leur reproduction. [Traduit par la Re´daction]

Introduction dinal migration may be advantageous because it allows mi- grants to exploit temporal or spatial variation in food Altitudinal migration is a common strategy of occupy- resources (Loiselle and Blake 1991; Solo´rzano et al. 2000), ing mountainous habitat but has been studied less intensively minimize the risk of nest predation (Boyle 2008; Fretwell than latitudinal migration (Berthold 2001; Newton 2008). For 1980), or escape extreme climatic conditions that impact phys- most altitudinal migrants seasonal movements are relatively iological function (Cox 1985). short and involve migrating uphill to breeding areas and Seasonal movements to higher elevation breeding sites can downhill to nonbreeding areas (Burgess and Mlingwa 2000; impose selection pressures that lead to elevation-specific life- Dingle 2004; Johnson and Maclean 1994; Stiles 1983). Altitu- history strategies. For example, a comparison of phylogeneti-

Received 11 November 2009. Accepted 11 February 2010. Published on the NRC Research Press Web site at cjz.nrc.ca on 10 March 2010. R.H. Mackas, D.J. Green,1 I.B.J. Whitehorne, E.N. Fairhurst,2 H.A. Middleton, and C.A. Morrissey.3 Centre for Wildlife Ecology, Department of Biological Sciences, Simon Fraser University, Burnaby, BC V5A 1S6, Canada. 1Corresponding author (e-mail: [email protected]). 2Present address: Department of Biology, Dalhousie University, Halifax, NS B3H 4J1, Canada. 3Present address: School of Biosciences, Cardiff University, Cardiff, UK.

Can. J. Zool. 88: 369–377 (2010) doi:10.1139/Z10-013 Published by NRC Research Press 370 Can. J. Zool. Vol. 88, 2010 cally paired avian taxa from low- and high-elevation sites in- and mountain streams. Dippers construct large domed nests dicates that high-elevation species have smaller clutches and 1–5 m above the water on cliff ledges, boulders, the ends of fewer broods per year than their low-elevation counterparts overhanging logs, in undercut banks, and on bridges (Badyaev and Ghalambor 2001). Badyaev and Ghalambor (Kingery 1996). Although both sexes contribute to territory (2001) found that the reduced fecundity in these high- defence, nest building, and the care of nestlings and fledg- elevation species is associated with increased parental care lings, only females incubate eggs and brood young. Dippers and a shift away from investment in offspring number toward will typically renest if a clutch or brood is lost early in the investment in offspring quality. Similar life-history trade-offs breeding season and may raise up to two broods per season have been described within species that breed on a steep- (Gillis et al. 2008; Kingery 1996; Price and Bock 1983). elevation gradient. For example, Dark-eyed Juncos (Junco We have studied an individually marked population of hyemalis (L., 1758)) that breed at high elevations initiate American Dippers in the Chilliwack River watershed, lo- breeding later and have a more compressed breeding season cated in the Cascade Mountain Range of southwestern Brit- than Dark-eyed Juncos breeding at low elevations, and conse- ish Columbia, Canada, from 1999 to 2009. This population quently produce fewer broods and fledglings per season. is composed of both altitudinal migrants and sedentary indi- However, Dark-eyed Juncos at high elevations produce heav- viduals (residents); approximately 85% of individuals are al- ier offspring with greater fat reserves than Dark-eyed Juncos titudinal migrants (Morrissey et al. 2004a). Adults rarely at low elevations (Bears et al. 2009). switch from being migratory to sedentary or vice versa, but Most populations of American Dippers (Cinclus mexicanus individuals frequently adopt a different strategy to their pa- Swainson, 1827) contain altitudinal migrants, individuals that rents (Gillis et al. 2008). Migrants overwinter with residents move between winter habitat on the coast or on rivers at low on the main stem of the Chilliwack River but move to elevations and breeding habitat on higher elevation streams higher elevation breeding sites on first- to third-order (Morrissey et al. 2004a; Price and Bock 1983; Willson and streams in the spring (February–April). On average, mi- Hocker 2008). Some populations contain both migratory and grants travel 6 km (range 2–21 km) and gain a mean of sedentary individuals, allowing the life-history consequences 226 m (range 10–735 m) as they move to higher elevation of altitudinal migration to be compared in a single population. territories in the breeding season (n = 33 birds; D.J. Green, In British Columbia, Canada, migrants consistently have unpublished data). Migrants have lower productivity (2.3 vs. lower productivity than residents because they initiate breed- 3.7 fledglings/year) but have higher annual survival (57.3% ing later and are consequently less likely to raise a second vs. 53.9%) than residents (Gillis et al. 2008). brood (Gillis et al. 2008; Morrissey 2004). Migrants, how- ever, have higher annual adult survival than residents (Gillis Monitoring reproduction and estimating nestling et al. 2008). Gillis et al. (2008) argued that migrants were condition making the ‘‘best of a bad job’’ when moving to higher eleva- tion breeding habitat, as the difference in adult survival was Breeding pairs were located by searching accessible sec- not sufficient to offset the lower productivity and the lifetime tions of the river and higher elevation creeks on foot, check- reproductive success of migrants was predicted to be lower ing suitable locations for nests, and following any dippers than that of residents. This argument, however, ignores the seen or heard. Breeding pairs were classed as sedentary if possibility that migrants in addition to having higher annual they occupied breeding territories on or within 1 km of the survival as adults may also compensate for their reduced fe- main stem of the Chilliwack River and were observed in the cundity by producing offspring of higher quality. same area during fall and winter. Pairs were classified as In this paper we assess whether breeding at higher eleva- migrants if they occupied breeding territories on creeks tions can lead to a shift in the life-history strategies of Amer- more than 1 km from the main stem of the river and were ican Dippers favouring the production of higher quality not observed on these territories in winter. Where possible rather than higher numbers of offspring. We assess whether nests were checked every 3–7 days to determine clutch ini- the seasonal movement of migrants enables them to exploit tiation dates, hatch dates, clutch and brood sizes, and the different prey and (or) provision at a higher rate than resi- fate of all nesting attempts. Precise hatch dates were calcu- dents using a combination of feeding observations, estimates lated using the nestling age at the first nest check after of energetic provisioning rates, and stable isotope analysis of hatching. Brood size and the mean nestling condition index juvenile feathers grown during the nestling period. Aquatic for each brood were determined when nestlings were larval invertebrates are the principal prey fed to nestling dip- banded, weighed, and measured 10–15 days (12.4 ± pers, but small fish are an alternative prey with higher ener- 2.0 days; mean ± SD) after hatching. The condition index getic content and nutritional value (Obermeyer et al. 2006). for each nestling was estimated using the residual from a We also examine whether differences in diet quality or provi- tarsus length – body mass regression. We were unable to es- sioning rate allow migratory dippers to compensate for their timate chick growth rates because of logistic difficulties as- lower annual fecundity by producing offspring that are in sociated with removing nestlings from nests located on cliffs better condition and (or) have higher postfledging survival. or bridges over fast-flowing rivers or streams multiple times. When nests were inaccessible, hatch dates were estimated Materials and methods by backdating from the date the brood fledged assuming that fledging occurs 25 days after hatching (Price and Bock Study species and site 1983). Brood size at these nests was assumed to equal the American dippers are aquatic that feed on number of fledglings observed during thorough searches of freshwater invertebrates and small fish in fast-flowing rivers the territory within 2 days of fledging.

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Feeding observations isotope analysis. Invertebrate samples, which were a composite We conducted feeding observations at 68 nests between of prey collected at each site, were rinsed with deionized water 2005 and 2008 (2005: n = 7; 2006: n = 22; 2007: n = 18; and oven dried at 40 8C for 48 h. Fish samples were rinsed with 2008: n = 21). Observations were conducted throughout the deionized water and freeze-dried for 48 h. Each fish and inver- day and varied in length from 30 to 200 min (66 ± 34 min; tebrate sample was then ground into homogenous powder and mean ± SD). All nests were observed midway through the subsamples of approximately 1 mg from each fish or inverte- nestling period when nestlings were 8–14 days of age, and brate sample were measured into miniature tin capsules 23 nests were also observed a second time late in the nestling (Costech Analytical Technologies, Inc., Valencia, California, period when nestlings were 17–24 days of age. During obser- USA) for isotopic analysis. vation periods we recorded when parents delivered food to We collected feather samples (the innermost right primary) the nest and the prey type and load size of each delivery. from a total of 63 juvenile dippers from 20 broods produced in Prey items were classified as aquatic invertebrates, fish eggs, 2008. Samples came from nestlings aged 11–14 days or re- and small fish. Deliveries of aquatic invertebrates were not cently fledged juveniles aged 25–40 days captured in mist defined more precisely because deliveries often include mul- nets set up across small channels in the natal territory. We pre- tiple prey taxa and we were often unable to identify the taxa pared feather samples for stable isotope analysis by removing being delivered. However, load sizes were classified as being the sheath from feathers that were not completely emerged, small, medium-sized, or large and were estimated in relation washing all feathers in a 2:1 chloroform and methanol solu- to the size of the bill. We subsequently grouped deliveries tion for 48 h, and air-drying them for a further 48 h. Samples into seven categories (Table 1). of approximately 1 mg were cut from the distal tip of each feather, weighed, and transferred into miniature tin capsules Prey and feather sampling for isotopic analysis. Prey and feather samples were collected so that we could (i) determine the mass and energetic content of the seven cat- Stable isotope analysis egories of food delivered to the nest and (ii) determine the Stable isotope ratios of nitrogen in the feather and prey stable isotope signatures of prey and feathers needed to calcu- samples were analysed at the Stable Isotope Facility, late the proportion of invertebrates and fish in the diet of University of California Davis, Davis, California, USA, using nestlings. We obtained larval aquatic invertebrate samples a PDZ Europa ANCA-GSL elemental analyzer interfaced to from six sites on the Chilliwack River and five sites on four a PDZ Europa 20–20 isotope ratio mass spectrometer (Sercon higher elevation creeks in 2008 by turning over rocks and Ltd., Cheshire, UK). Sample nitrogen isotope ratios were collecting all macroinvertebrates >2 mm long by hand. Each compared with those in air. Values for 15N were calculated sample included plectopteran and ephemopteran nymphs and and reported using the standard delta (d) notation in parts per trichopteran larvae, all of which are preyed on by dippers thousand (%). During analysis, samples were interspersed (Bakus 1959; Mitchell 1968). Samples of salmonid fry were with replicate laboratory standards that had been previously collected from the Chilliwack River and three creeks using a calibrated against NIST Standard Reference Materials dip net. We targeted fish of the size observed during (IAEA-N1, IAEA-N2, IAEA-N3, IAEA-CH7, and NBS-22). provisioning observations (~40 mm long). All fish sampled Measurement error was ±0.1%. were either coho salmon (Oncorhynchus kisutch (Walbaum, 1792)) or steelhead (Oncorhynchus mykiss (Walbaum, 1792)). Invertebrate and fish samples were stored in ethanol prior to Postfledging survival being transferred to the laboratory. We examined the postfledging survival of all banded nest- We calculated the energetic value of small, medium-sized, lings known to have fledged between 1999 and 2008 (n = and large invertebrate deliveries by preparing 11 prey sub- 526). Survival from fledging until the end of January the samples representative of each load size, determining their following year was assessed using resighting data obtained dry mass, and converting these mass to energetic values during systematic censuses of the Chilliwack River conducted using published values for aquatic invertebrates (Table 1). five times a year between November 1999 and July 2009, Invertebrate subsamples contained multiple prey with individ- detailed searches of the main stem of the river and higher ele- uals from each major taxa being combined to create load sizes vation tributaries conducted each breeding season (2000– that approximated invertebrate deliveries made by dippers, 2009), and regular visits to the study area made to capture using tweezers with marks corresponding to 1/4, 1/2, and 1 and mark breeding and wintering adults (for more details see bill length as a reference. Invertebrate subsamples Gillis et al. 2008). Our use of juvenile survival to assess the were rinsed with deionized water and oven dried at 40 8C for quality of offspring raised by migrants and residents could be approximately 48 h prior to weighing. We estimated the ener- biased if the offspring of migrants disperse farther, are more getic content of fish or steelhead eggs delivered to nestlings likely to disperse outside the watershed, and are less likely to using published data on the size–mass relationship and ener- be detected. However, we believe that any resighting bias is getic content for juvenile salmon or salmonid eggs (Table 1). likely to be small because the offspring of migrants Fish fed to nestlings were approximately twice the bill length overwinter with the offspring of residents on the main stem of an adult dipper, so fish were assumed to be 44 mm long. of the river, the migratory strategy of an individual cannot be Energetic values for the different prey types and load sizes predicted by the strategy of their parents, and the distance were then used to calculate the energetic provisioning rate from the natal territory to the point individuals are resighted (kJ/h) during each provisioning observation. is small compared with the length of the study area (Gillis et We also prepared invertebrate and fish samples for stable al. 2008; Middleton and Green 2008).

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Data analysis We conducted a total of 91 provisioning observations at 68 nests containing broods produced by 54 pairs and deter- mined the mean nestling condition of 59 broods produced by 34 pairs. We therefore used a mixed modeling approach to test whether migrants provide their offspring with a higher quality diet, deliver food at a higher rate, and produce higher quality offspring than residents. We examined five independent variables: the proportion of deliveries that con- (fish and invertebrates) 7.21 6.82 tained fish, whether at least one fish was delivered during a ) broods. provisioning observations (yes or no), the delivery rate of both parents (total number of feeding visits/h), the energetic

delivery. The references give estimates for provisioning rate (kJ/h), and the average nestling condition of a brood. Pair identity was included as a random term in { all models. We included six explanatory variables in each (fish) 4.40 — 1.11 model: migratory strategy, hatch date, year, brood-size cate-

Cinclus mexicanus gory (small = 1 or 2; medium-sized = 3; large = 4 or 5), nestling age, and the time of day observations were con- ducted (morning 0800–1200; midday 1200–1600; afternoon 1600–2000). Brood size was categorized as a factor with three levels, as brood sizes of 1 and 5 were rare. For each analysis, we initially fitted a full model including all main || (invertebrates) effects and interaction terms, and then sequentially elimi- Energetic content 22.9 —7.8 4.40 nated all nonsignificant interactions and then main effects until only significant terms remained. To ensure that the or- der in which terms were dropped did not influence the final model selected, we re-evaluated any term eliminated by add-

{ § ing and dropping it from the final reported model. We as-

(fish) sessed the significance of terms in models by using the 1.55 change in deviance or the Wald statistic associated with dropping individual terms from models. Both the change in deviance and the Wald statistic approximate a c2 distribu- tion. Estimates of effects and predicted means are presented with standard errors. We used generalized linear mixed models (GLMM) to in-

(invertebrates) vestigate how nestling condition and the migratory strategy 0.017 (altitudinal migrant or resident) of their parents influenced the postfledging survival of 526 fledglings produced by 104 pairs. Pair identity was included as a random term. Models were fitted to examine the relationship between survival and migratory strategy, survival and nestling condition, and survival and migratory strategy after controlling for nestling condition, year, and hatch date. Significance of explanatory terms was evaluated using the Wald statistic. All models were fitted using GenStat version 11 (VSN International

bill length 0.169 — 22.9Ltd., Hemel Hempstead, — UK). 3.87 bill length (invertebrates) bill length 0.017 — 22.9* — 0.39

We used a two-source standard linear mixing model bill length 0.407 — 22.9 — 9.32

15

(Phillips 2001) and the d N values obtained from the prey bill length — 1.55 bill length (fish) and bill length —and 3.10 feather samples — to estimate 4.40 the relative 13.64 contribution <0.25 fish and invertebrates make to the diet of individual nest- lings. We used habitat specific d15N for the two prey types as mean isotope values differed (see Results) and a discrim- ination factor (fractionation value) of 2.91%. This is the mean discrimination factor across all tissue types from 52 studies to have estimated –diet discrimination factors in birds (Caut et al. 2009), and matches the value (2.91%) used in a previous study of diet composition of adult dippers Categories (defined by prey type and load size relative to bill length) used to classify prey delivered to American Dipper (

Representative samples were used to estimate dry mass (invertebrates) or wet mass (fish and eggs) and the energetic value associated with each type of (Morrissey et al. 2004b). We then compared the relative contribution fish make to the diet of nestlings provisioned Value from Chingbu 2001. Value averaged from dataValue reported from in Rombough Boldt 1988. and Haldorson 2004 and Dempson et al. 2004. Value from Hendry and Berg 1999. Note: *Value averaged from data reported in Brey et al. 1988 and Obermeyer et al. 2006. { { § || by migratory and sedentary parents using a mixed model One fish 2 Large invertebrates >0.5 Medium-sized invertebrates 0.25–0.5 Prey deliveredSmall invertebrates <0.25 Load size Dry mass (g) Wet mass (g) kJ/g dry mass kJ/g wet mass Energetic value (kJ/delivery) Salmon egg — — 0.14 One fish and invertebrates 2 Two fish 2 Table 1. the mass and (or) energetic content of particular prey types. with pair (= brood) identity entered as a random term.

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Results visioning rates, however, did not vary significantly across 2 years or with the time of day (year: c½3 = 1.8, p = 0.61; Nestling diet 2 period: c½2 = 1.4, p = 0.50). Provisioning rates also did not American Dippers delivered larval aquatic invertebrates, 2 increase with brood size (c½2 = 1.72, p = 0.43), although the small fish, and occasionally, salmonid eggs to their broods. trend was for provisioning rates to increase with brood size, The proportion of deliveries that included one or more fish or vary with brood age (c2 = 1.6, p = 0.21). Despite the did not vary with the size or age of the brood (brood size: ½1 lower overall delivery rates, residents had a higher provi- c2 = 0.4, p = 0.84; age: c2 = 0.6, p = 0.44). The ½2 ½1 sioning rate than migrants because a greater proportion of proportion of deliveries that included fish declined across 2 2 their deliveries included fish (c½1 = 7.3, p = 0.008; Fig. 1c). the season (date effect: –0.29 ± 0.11; c½1 = 6.5, p = 0.01) but did not vary with the time of day or between years Nestling quality (period: c2 = 4.7, p = 0.10; year: c2 = 1.2, p = 0.77). After ½2 ½3 We were able to access and therefore calculate a mean controlling for seasonal variation, resident pairs fed their nestling condition index for 59 of the 71 intensively moni- broods a diet that contained a greater proportion of fish 2 tored broods. Two factors had an effect on the mean nestling than did migratory pairs (c½1 = 8.7, p = 0.004; Fig. 1a). condition index of these broods. Nestlings in broods raised This pattern remained when we analysed the diet fed to dip- by residents were in better condition than nestlings in broods per broods as a binomial variable (fish: yes or no) with the raised by migrants (c2 = 4.0, p = 0.05; Fig. 1d). Nestlings duration of the focal observation entered as a covariate ½1 2 were also in better condition in 2006 and 2007 than in 2005 (GLMM; duration of observation: c½1 = 3.4, p = 0.07; mi- and 2008 (2005: –0.56 ± 0.31; 2006: 0.24 ± 0.22; 2007: gratory strategy: residents = 0.58 ± 0.06, migrants 0.21 ± 0.22 ± 0.25; 2008: –0.48 ± 0.19; c2 = 11.6, p = 0.02). De- 2 ½3 0.08; c½1 = 8.0, p = 0.006). spite seasonal declines in provisioning rates, the mean nest- Larval aquatic invertebrate and fish samples collected ling condition index of a brood was independent of hatch from the river had more enriched d15N signatures than those 2 date (c½1 = 0.4, p = 0.84). This was not a result of seasonal collected from higher elevation tributaries (Table 2). Feather declines in brood size; brood size did not vary with hatch samples from juvenile dippers provisioned by residents on 2 15 date (date effect: –0.003 ± 0.005; c½1 = 0.17, p = 0.68). the river also had more enriched d N signatures than feath- The mean nestling condition index of a brood also did not ers from juveniles provisioned by migrants on the tributaries vary significantly with brood size (c2 = 3.2, p = 0.21), (Table 2). The linear mixing model using habitat-specific ½2 although nestlings in large broods were in slightly worse d15N values for fish and invertebrates estimated the amount condition than nestlings in small and medium-sized broods of fish in the diet of nestlings to vary from 0% to 83%. Ju- (model predictions (mean ± SE) controlling for migratory veniles fed by sedentary pairs had a diet containing almost strategy and year; small broods: 0.02 ± 0.29; medium-sized three times as much fish as juveniles fed by migratory pairs broods: 0.10 ± 0.23; large broods: –0.30 ± 0.17). (percentage (mean ± SD) of fish in diet: sedentary off- spring = 32% ± 22% (n = 40); migratory offspring = 11% ± Postfledging survival 6% (n = 23); c2 = 14.9, p < 0.001). ½1 Eleven percent of offspring that fledged (n = 526) between 1999 and 2008 were known to survive until the end of Delivery rates January following their hatch year. Fledglings produced by Pairs of American Dippers delivered prey to broods approx- residents were three times as likely as fledglings produced imately 16 times/h (range 4–44 times/h) when nestlings were by migrants to survive their first winter (residents: 0.12 ± between 9 and 23 days of age. Delivery rates increased with c2 p brood size (small broods: 11.0 ± 1.9 deliveries/h; medium- 0.02; migrants: 0.04 ± 0.02; ½1 = 4.1, = 0.04). The higher sized broods: 16.5 ± 1.5; large broods: 19.5 ± 1.3; c2 =15.5, postfledging survival of offspring produced by residents was ½2 due, in part, to being in better condition because nestling p < 0.001) but did not vary with nestling age (c2 =0.2,p = ½1 condition had a positive effect on survival (nestling condi- 0.68). Delivery rates also varied between years (2005: 14.9 ± tion: c2 = 8.3, p = 0.004; Fig. 2). Postfledging survival also 2 deliveries/h; 2006: 19.8 ± 1.4 deliveries/h; 2007: 14.2 ± ½1 2 1.8 deliveries/h; 2008: 13.8 ± 1.4 deliveries/h; c2 =11.3,p = varied between years (c½8 = 17.0, p = 0.03) but was not re- ½3 2 0.01) but did not vary with the time of day or across the season lated to hatch date (c½1 = 1.9, p = 0.17). After controlling for 2 2 nestling condition and year, postfledging survival did not (period: c½2 =1.1,p = 0.59; hatch date: c½1 =0.07,p =0.79). After controlling for brood size and interannual variation, mi- vary with the migratory strategy of the parents (model pre- gratory pairs had a higher delivery rate than resident pairs dictions (mean ± SE); residents: 0.11 ± 0.01; migrants: 2 2 0.05 ± 0.03; c 1 = 1.7, p = 0.19). (c½1 =5.9,p = 0.02; Fig. 1b). ½

Energetic provisioning rate Discussion The energetic provisioning rate to the brood, estimated in Breeding at higher elevations can compress the breeding kJ/h, increased with both the parental delivery rate and the season, reducing the number of clutches that can be initiated proportion of deliveries that included fish (delivery rate: or broods that can be raised and select for investment in off- 2 2 c½1 = 29.4, p < 0.001; proportion fish: c½1 = 144.9, p < spring quality rather than offspring number (Badyaev and 0.001). Provisioning rates consequently declined across the Ghalambor 2001; Bears et al. 2009). The association between 2 season (date effect: –1.59 ± 0.60; c½1 = 7.5, p = 0.008). Pro- breeding elevation and productivity is observed in American

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Fig. 1. Relation between migratory strategy and (a) the percentage of deliveries made to the nest with food that contained one or more fish, (b) the combined delivery rate of male and female American Dippers (Cinclus mexicanus) when provisioning nestlings, (c) the energetic provisioning rate (kJ/h), and (d) the mean nestling condition index of broods when banded at approximately 12 days of age. The bars show the model predictions (mean + SE) controlling for date in a and c, brood size and year in b, and year in d.

Table 2. Summary of isotopic values (mean ± SD) from prey and American Dipper (Cinclus mex- icanus) feather samples.

d15N(%)(n) Statistics River Tributary t c2 df p Aquatic invertebrates 3.66±2.43 (6) 0.39±0.79 (5) 2.85 — 9 0.02 Salmon fry 11.53±1.58 (6) 9.89±0.88 (6) 2.2 — 10 0.05 Feather 9.04±1.78 (40) 4.39±0.73 (23) — 139 1 <0.001 Note: Prey samples were collected from six sites on the main stem of the Chilliwack River and six sites on higher elevation creeks. Feather samples were obtained from nestlings provisioned by 12 sedentary pairs on the Chilliwack River and 8 migratory pairs on the tributaries.

Dippers; individuals that migrate to higher elevations to evations. Species breeding at higher elevations did not pro- breed are less likely to initiate a second clutch following the vision at a higher rate but provided fledged young with success of their first breeding attempt and produce less off- food for considerably longer than species breeding at low el- spring than sedentary individuals that breed at lower eleva- evations. Extended postfledging care has been linked to tions (Gillis et al. 2008; Morrissey 2004). However, we higher juvenile survival and recruitment in several species found no evidence migratory individuals trade off the number (e.g., Green and Cockburn 2001; Middleton and Green of offspring produced over the course of a season with off- 2008), suggesting reduced fecundity could be compensated spring quality. Migrants fed their offspring less fish and, for by higher juvenile survival. Similarly, Bears et al. although they compensated by feeding at a higher rate, had (2009) found that while Dark-eyed Juncos breeding at high lower energetic provisioning rates. Nestlings in broods raised elevations produced fewer offspring their offspring were in by migrants also had a lower mean nestling condition index better condition and more likely to survive until 25–30 days than nestlings in broods raised by residents and, as a conse- of age. In contrast, we found little evidence that breeding at quence, fledglings produced by migrants were less likely to higher elevations is associated with greater parental care and survive their first winter. (or) the production of offspring with higher juvenile survival Comparative studies have documented shifts in the life in American Dippers. Dippers breeding at higher elevations histories of species and populations breeding at higher ele- had lower energetic provisioning rates than sedentary con- vations that result in a trade-off between the number and specifics at lower elevations and produced offspring that the quality of young produced. For example, Badyaev and were in worse condition that were less likely to survive until Ghalambor (2001) found a strong negative relationship be- the following year. This differs slightly from previous work, tween the number of offspring and the level of parental care which included a considerable amount of data from 2000 in phylogenetically paired taxa breeding at high and low el- when reproductive success was at a 10 year high, that

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Fig. 2. Relation between American Dipper (Cinclus mexicanus) Reduction in the amount of fish fed to nestling dippers nestling condition, estimated as the residual of a mass–tarsus re- could also be due to seasonal changes in the abundance and gression, and the probability of being resighted after the end of distribution of young salmonids, increased flow rates and January of the following year. The line shows the model predic- turbidity owing to the spring snowmelt that makes foraging tions, the circles show the data binned into 2 g categories commen- for fish more difficult, or seasonal increases in the abun- cing at –12 g, and the numbers next to the circles show the sample dance and (or) availability of aquatic invertebrates (Bram- size within each category. blett et al. 2002; Crisp 2000). Seasonal variation in provisioning behavior did not, however, lead to a corre- sponding seasonal decline in the mean nestling condition in- dex of a brood. This result was not due to seasonal declines in brood size. The mean nestling condition index may have remained constant because the rising temperature (mean minimum and maximum daily temperatures for the Chilli- wack River hatchery: 1 April = 2.8 and 10.7 8C; 30 June = 10.7 and 21.3 8C; National Climate Data and Information Archive, Environment Canada, Fredericton, New Brunswick, Canada) reduced thermoregulatory costs and nestling ener- getic demands (see Dawson et al. 2005). We also found no evidence for a negative relationship between hatch date and postfledging survival in American Dippers, in contrast to several other studies on passerines (reviewed in Daan et al. 1989). The higher survival of offspring raised by residents therefore appears to be due more to differences in nestling condition resulting from being fed a higher quality diet than reported no difference in the mean nestling mass of broods differences in hatch date that allow their offspring more raised by migratory and sedentary dippers (Morrissey 2004). time to develop foraging skills prior to winter. Importantly, however, neither study provides any evidence Altitudinal migration may allow individuals to track spa- to suggest dippers produce better quality offspring if they tial and temporal variation in food availability (Loiselle and migrate to higher elevations to breed. Blake 1991; Solo´rzano et al. 2000), or allow individuals to Breeding at higher elevations may not have been associ- reduce the risk of nest predation (Boyle 2008; Fretwell ated with increased parental care in this study because pa- 1980). Neither hypothesis appears to be a plausible explana- rental care was only examined during the nestling period. tion for altitudinal migration in American Dippers. Feeding This is unlikely to be the case because parental provisioning observations and stable isotope analysis of feather samples, rates decline considerably 1 week after fledging in American which reflect nestling diet over a longer period, show that Dippers, and the offspring of migrants and residents are offspring of migrants have a diet containing more inverte- equally likely to have left their natal territory within 2 weeks brates and less fish than the offspring of residents. This re- (Middleton et al. 2007; Middleton and Green 2008). Further- sult is counter to what would be expected if altitudinal more, the positive correlation between our index of nestling migration gave migratory dippers access to a higher quality condition and postfledging survival in this population sug- diet or allowed higher energetic provisioning rates because gests that postfledging parental care does not compensate fish have a higher energetic content and nutritional value for differences in the level of care provided during the nest- (percent protein, phosphorus, and calcium) than aquatic in- ling period. The absence of a trade-off between fecundity vertebrates (Obermeyer et al. 2006), and nestlings fed a diet and parental care or juvenile survival suggests that life- that contains more fish are in better condition (Obermeyer et history variation in this species is driven more by ecological al. 2006; this study). Previous work suggests it is also un- factors, such as intraspecific competition, than selection likely that altitudinal migration allows dippers to reduce the pressures exerted by the different conditions at different ele- level of nest predation. Morrissey (2004) found that nests of vations. migratory dippers are as likely to fail owing to predation as Our work has demonstrated that ecological conditions at nests of residents. high and low elevation influence both the number and the Altitudinal migration in species with alternative migratory quality of offspring produced by migratory and sedentary strategies may be an outcome of intraspecific competition. American Dippers (Gillis et al. 2008; Morrissey 2004; this For example, in Carolina Juncos (Junco hyemalis carolinen- study). Seasonal variation in ecological conditions might sis Brewster, 1886) competition for food at high elevations also be expected to lead to seasonal variation in delivery during the winter has been argued to force subordinate indi- rates, nestling diet, nestling condition, and postfledging sur- viduals to migrate to lower elevations (Rabenold and Rabe- vival. In this study we observed seasonal declines in the pro- nold 1985). In contrast, altitudinal migration in American portion of deliveries that included fish and showed that this Dippers has been argued to be an outcome of intraspecific led to seasonal declines in energetic provisioning rates of competition for limited nesting sites at low elevations that both residents and migrants. This may reflect differences in forces the majority of individuals to either move to higher parental age and foraging ability, as young birds often ini- elevations to breed or forgo reproduction (Gillis et al. tiate breeding later than old birds (Martin 1995) and may be 2008). This hypothesis is supported by work showing that less proficient foragers than older birds (Wunderle 1991). distributions of dippers are limited by suitable nest sites

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(Loegering and Anthony 2006), residents have consistently eastern Alaska drainage basin. Trans. Am. Fish. Soc. 131(3): higher annual productivity than migrants, and are predicted 498–506. doi:10.1577/1548-8659(2002)131<0498:SUOSTA>2.0. to have higher lifetime reproductive success (Gillis et al. CO;2. 2008). This study demonstrates migrants do not compensate Brey, T., Rumohr, H., and Ankar, S. 1988. Energy content of for their lower productivity by producing higher quality macrobenthic invertebrates: general conversion factors from young. In fact, differences in the lifetime reproductive suc- weight to energy. J. Exp. Mar. Biol. Ecol. 117(3): 271–278. cess of migrants and residents will have been underesti- doi:10.1016/0022-0981(88)90062-7. mated because migrants produce lower quality offspring Burgess, N.D., and Mlingwa, C.O.F. 2000. Evidence for altitudinal migration of forest birds between montane Eastern Arc and low- that are less likely to survive their first winter. This study land forests in East Africa. Ostrich, 71: 184–190. therefore provides additional support for the hypothesis that Caut, S., Angulo, E., and Courchamp, F. 2009. Variation in discri- altitudinal migration is a conditional strategy and that mi- mination factors (D15N and D13C): the effect of diet isotopic va- grants are subordinate birds that are simply making the lues and applications for diet reconstruction. J. Appl. Ecol. ‘‘best of a bad job’’ (Adriaensen and Dhondt 1990) by mov- 46(2): 443–453. doi:10.1111/j.1365-2664.2009.01620.x. ing to higher elevations to breed. Chingbu, P. 2001. Occurrence and distribution of Salmincola californiensis (Copepoda: Lernaeopodidae) on juvenile sockeye Acknowledgements salmon (Oncorhynchus nerka) in Lake Washington. J. Freshwat. We thank M. Bandura, D. Lissimore, R. McKibbin, I. Pol- Ecol. 16: 615–620. Cox, G.W. 1985. The evolution of avian migration systems be- let, J. Preston, C. Rothenbach, and A. Potvin for their efforts tween temperate and tropical regions of the New World. Am. in the field; E. Krebs and E. Gillis for contributing provi- Nat. 126(4): 451–474. doi:10.1086/284432. sioning data; R. Brown and the employees of the Chilliwack Crisp, D.T. 2000. Trout and salmon: Ecology, conservation, and re- River Rafting Company, who took us to nests that would habilitation. Fishing News Books, Oxford. have otherwise been inaccessible; and V. Magnusson and Daan, S., Dijkstra, C., Drent, R.H., and Meijer, T. 1989. Food staff for accommodation at Cultus Lake Salmon Research supply and the annual timing of avian reproduction. Proc. Int. Laboratory. Comments by Elsie Krebs and an anonymous Ornithol. Congr. 19: 392–407. reviewer helped improved the paper. Funding for this study Dawson, R.D., Lawrie, C.C., and O’Brien, E.L. 2005. The impor- was provided by a Natural Sciences and Engineering Re- tance of microclimate variation in determining size, growth and search Council of Canada (NSERC) Undergraduate Student survival of avian offspring: experimental evidence from a cavity Research Award (R.H.M.), a NSERC Discovery Grant nesting . Oecologia (Berl.), 144(3): 499–507. doi:10. (D.J.G.), a NSERC Canada Graduate Scholarship M Exten- 1007/s00442-005-0075-7. sion (I.B.J.W.), and Environment Canada, through the Geor- Dempson, J.B., Schwarz, C.J., Shears, M., and Furey, G. 2004. gia Basin Ecosystem Initiative (C.A.M.). All field protocols Comparative proximate body composition of Atlantic salmon were approved by the Simon Fraser University Animal Care with emphasis on parr from fluvial and lacustrine habitats. J. Committee and conducted under a Federal Scientific Permit. Fish Biol. 64(5): 1257–1271. doi:10.1111/j.0022-1112.2004. 00389.x. References Dingle, H. 2004. The Australo-Papuan migration system: another consequences of Wallace’s Line. Emu, 104(2): 95–108. doi:10. Adriaensen, F., and Dhondt, A.A. 1990. Population dynamics and 1071/MU03026. partial migration of the European Robin (Erithacus rubecula)in Fretwell, S.D. 1980. Evolution of migration in relation to factors different habitats. J. Anim. Ecol. 59(3): 1077–1090. doi:10.2307/ regulating numbers. In Migrant birds in the Neotropics. 5033. Edited by A. Keast and E.S. Morton. Smithsonian Institute Badyaev, A.V., and Ghalambor, C.K. 2001. Evolution of life his- Press, Washington, D.C. pp. 517–527. tories along elevational gradients: trade-off between parental Gillis, E.A., Green, D.J., Middleton, H.A., and Morrissey, C.A. care and fecundity. Ecology, 82(10): 2948–2960. doi:10.1890/ 2008. Life history correlates of alternative migratory strategies 0012-9658(2001)082[2948:EOLHAE]2.0.CO;2. in American Dippers. Ecology, 89(6): 1687–1695. doi:10.1890/ Bakus, G.T. 1959. Observations on the life history of the Dipper in 07-1122.1. PMID:18589532. Montana. Auk, 76(2): 190–207. Green, D.J., and Cockburn, A. 2001. Post-fledging care, philopatry Bears, H., Martin, K., and White, G.C. 2009. Breeding in high- and recruitment in brown thornbills. J. Anim. Ecol. 70(3): 505– elevation habitat results in shift to slower life-history strategy 514. doi:10.1046/j.1365-2656.2001.00503.x. within a single species. J. Anim. Ecol. 78(2): 365–375. doi:10. Hendry, A.P., and Berg, O.K. 1999. Secondary sexual characters, 1111/j.1365-2656.2008.01491.x. PMID:19007385. energy use, senescence, and the cost of reproduction in sockeye Berthold, P. 2001. : a general survey. 2nd ed. Oxford salmon. Can. J. Zool. 77(11): 1663–1675. doi:10.1139/cjz-77- University Press, Oxford. 11-1663. Boldt, J.L., and Haldorson, L.J. 2004. Size and condition of wild Johnson, D.N., and Maclean, G.L. 1994. Altitudinal migration in and hatchery pink salmon juveniles in Prince William Sound, Natal. Ostrich, 65: 86–94. Alaska. Trans. Am. Fish. Soc. 133(1): 173–184. doi:10.1577/ Kingery, H.E. 1996. American Dipper (Cinclus mexicanus). In The T02-138. birds of North America. No. 229. Edited by A. Poole and F. Boyle, W.A. 2008. Can variation in risk of nest predation explain Gill. Academy of Natural Sciences, Philadelphia, Pa., and Amer- altitudinal migration in tropical birds? Oecologia (Berl.), ican Ornithologists’ Union, Washington, D.C. 155(2): 397–403. doi:10.1007/s00442-007-0897-6. Loegering, J.P., and Anthony, R.G. 2006. Nest-site selection and Bramblett, R.G., Bryant, M.D., Wright, B.E., and White, R.G. productivity of American dippers in the Oregon Coast Range. 2002. Seasonal use of small tributary and main-stem habitats by Wilson J. Ornithol. 118(3): 281–294. doi:10.1676/04-100.1. juvenile steelhead, coho salmon, and Dolly Varden on a south- Loiselle, B.A., and Blake, J.G. 1991. Temporal variation in birds

Published by NRC Research Press Mackas et al. 377

and fruits along an elevational gradient in Costa Rica. Ecology, Obermeyer, K.E., White, K.S., and Willson, M.F. 2006. Influence 72(1): 180–193. doi:10.2307/1938913. of salmon on the nesting ecology of American dippers in south- Martin, K. 1995. Patterns and mechanisms for age dependent repro- eastern Alaska. Northwest Sci. 80(1): 26–33. duction in birds. Am. Zool. 35(4): 340–348. Phillips, D.L. 2001. Mixing models in analyses of diet using multi- Middleton, H.A., and Green, D.J. 2008. Correlates of postfledging ple stable isotopes: a critique. Oecologia (Berl.), 127(2): 166– survival, the timing of dispersal, and local recruitment in Ameri- 170. doi:10.1007/s004420000571. can Dippers. Can. J. Zool. 86(8): 875–881. doi:10.1139/Z08-069. Price, F.E., and Bock, C.E. 1983. Population ecology of the Dipper Middleton, H.A., Green, D.J., and Krebs, E.A. 2007. Fledgling (Cinclus mexicanus) in the Front Range of Colorado. Stud. begging and parental responsiveness in American dippers Avian Biol. 7: 1–89. (Cinclus mexicanus). Behaviour, 144(5): 485–501. doi:10.1163/ Rabenold, K.N., and Rabenold, P.P. 1985. Variation in altitudinal 156853907780713064. migration, winter segregation, and site tenacity in two subspe- Mitchell, P.A. 1968. The food of the Dipper (Cinclus mexicanus cies of dark-eyed juncos in the southern Appalachians. Auk, Swainson) on two western Montana streams. M.Sc. thesis, Uni- 102(4): 805–819. versity of Montana, Missoula. Rombough, P.J. 1988. Growth, aerobic metabolism, and dissolved Morrissey, C.A. 2004. Effect of altitudinal migration within a wa- oxygen requirements of embryos and alevins of steelhead, Salmo tershed on the reproductive success of American dippers. Can. J. gairdneri. Can. J. Zool. 66(3): 651–660. doi:10.1139/z88-097. Zool. 82(5): 800–807. doi:10.1139/z04-042. Solo´rzano, S., Castillo, S., Valverde, T., and A´ vila, L. 2000. Quet- Morrissey, C.A., Bendell-Young, L.I., and Elliott, J.E. 2004a. Sea- zal abundance in relation to fruit availability in a cloud forest of sonal trends in population density, distribution, and movement southern Mexico. Biotropica, 32(3): 523–532. of American dippers within a watershed of southwestern British Stiles, F.G. 1983. Birds. In Costa Rican Natural History. Edited by Columbia, Canada. Condor, 106(4): 815–825. doi:10.1650/7455. D.H. Janzen. University of Chicago Press, Chicago. pp. 502– Morrissey, C.A., Bendell-Young, L.I., and Elliott, J.E. 2004b. Link- 530. ing contaminant profiles to the diet and breeding location of Willson, M.F., and Hocker, K.M. 2008. American dippers winter- American dippers using stable isotopes. J. Appl. Ecol. 41(3): ing near Juneau, Alaska. Northwest. Nat. 89(1): 24–32. doi:10. 502–512. doi:10.1111/j.0021-8901.2004.00907.x. 1898/1051-1733(2008)89[24:ADWNJA]2.0.CO;2. Newton, I. 2008. The migration ecology of birds. Academic Press, Wunderle, J.M. 1991. Age-specific foraging proficiency in birds. London. Curr. Ornithol. 3: 273–324.

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